Derry City Football Club was founded in 1928 (refounded 2010) and has spent the majority of its time in the League of Ireland in the Premier Division, the top tier of league football in the Republic of Ireland. However, the club was expelled in November 2009 when it was discovered there were secondary, unofficial contracts with players. Derry were reconstituted a few weeks later and readmitted to the First Division.

Derry City are the League of Ireland's only participant from Northern Ireland. They play their home fixtures at the Brandywell Stadium and the players wear red and white striped shirts from which their nickname, the Candystripes, derives.

The club initially played in the Irish League, the domestic league in Northern Ireland, and won a title in 1964–65. In 1971 security concerns related to unrest in Northern Ireland meant matches could not be played at the Brandywell. The team played "home" fixtures 30 miles (48 km) away in Coleraine. Security forces withdrew their objections to the use of the Brandywell the following year, but in the face of insistence from the Irish League that the unsustainable arrangement continue, the club withdrew from the league.

After 13 years in junior football Derry joined the League of Ireland's new First Division in 1985/86. Derry won the First Division title in 1987 and achieved promotion to the Premier Division where they remained until 2009, being relegated as a result of financial problems rather than poor sporting performance. The club won a domestic treble in 1988–89, the only Irish club to ever do so.

League Champions:Twice
1988/89, 1996/97.

First Division Champions: Twice
1986/87, 2010.

FAI Cup Winners: Five times
1988/89, 1994/95, 2002, 2006, 2012.

League Cup Winners: Eleven times
1988/89, 1990/91, 1991/92, 1993/94, 1999/00, 2005, 2006, 2007, 2008, 2011, 2018.